The function of androgen/androgen receptor and insulin growth factor‑1/insulin growth factor‑1 receptor on the effects of Tribulus terrestris extracts in rats undergoing high intensity exercise

Wu,Yin; Yang,Hongfang; Wang,Xiaohui

doi:10.3892/mmr.2017.6891

The function of androgen/androgen receptor and insulin growth factor‑1/insulin growth factor‑1 receptor on the effects of Tribulus terrestris extracts in rats undergoing high intensity exercise

Authors:
- Yin Wu
- Hongfang Yang
- Xiaohui Wang
View Affiliations

Affiliations: Department of Computer and Statistics, Shanghai University of Sport, Shanghai 200438, P.R. China, School of Kinesiology, Shanghai University of Sport, Shanghai 200438, P.R. China
Published online on: June 30, 2017 https://doi.org/10.3892/mmr.2017.6891
Pages: 2931-2938

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Our previous study demonstrated that treatment with Tribulus terrestris (TT) extracts (120 mg/kg) promoted the muscle weight gain and performance of rats undergoing high intensity exercise. The present study was designed to explore the mechanisms underlying the effect of treatment with TT extracts and the involvement of androgens, the androgen receptor (AR), insulin growth factor‑1 (IGF‑1) and the IGF‑1 receptor (IGF‑1R). A total of 32 Sprague‑Dawley rats were randomly divided into groups as follows: Control; TT, treated with TT extracts, E, high intensity exercise; E+TT, high intensity exercise plus TT treatment. The rats of the E and E+TT groups underwent high intensity exercise with a progressively increasing load for 5 weeks, and TT extracts were intragastrically administered in the TT and E+TT rats 30 min prior to training. TT extract composition was analyzed using ultra‑high performance liquid chromatography‑quadrupole‑time of flight mass spectrometry. Testosterone and IGF‑1 plasma levels and AR, IGF‑1R and myosin heavy chain (MHC) protein levels in muscles were determined by ELISA and western blotting, respectively. The saponins tigogenin and diosgenin comprised ~71.35% of the total peak area. Compared with the E group, TT extracts increased the testosterone and IGF‑1 plasma levels, and AR, IGF‑1R and MHC protein levels in the gastrocnemius of rats undergoing high intensity exercise, accompanied with increased body weight and gastrocnemius weight. In conclusion, the effect of TT extracts on the performance of high intensity exercise rats may be attributed to increased levels of circulating testosterone and IGF‑1 and increased AR and IGF‑1R protein expression levels in the gastrocnemius, resulting in increased muscle weight and increased MHC in the gastrocnemius. The present study provided preliminary evidence supporting the use of TT extracts as a dietary supplement for the promotion of skeletal muscle mass increase and the enhancement of athletic performance in humans performing high intensity exercise.

View Figures

View References

1	Velders M and Diel P: How sex hormones promote skeletal muscle regeneration. Sports Med. 43:1089–1100. 2013. View Article : Google Scholar : PubMed/NCBI
2	Schoenfeld BJ: Postexercise hypertrophic adaptations: A reexamination of the hormone hypothesis and its applicability to resistance training program design. J Strength Cond Res. 27:1720–1730. 2013. View Article : Google Scholar : PubMed/NCBI
3	Wood RI and Stanton SJ: Testosterone and sport: Current perspectives. Horm Behav. 61:147–155. 2012. View Article : Google Scholar : PubMed/NCBI
4	Di Luigi L, Romanelli F, Sgrò P and Lenzi A: Andrological aspects of physical exercise and sport medicine. Endocrine. 42:278–284. 2012. View Article : Google Scholar : PubMed/NCBI
5	Bassil N, Alkaade S and Morley JE: The benefits and risks of testosterone replacement therapy: A review. Ther Clin Risk Manag. 5:427–448. 2009.PubMed/NCBI
6	El-Tantawy WH, Temraz A and El-Gindi OD: Free serum testosterone level in male rats treated with Tribulus alatus extracts. Int Braz J Urol. 33:554–559. 2007. View Article : Google Scholar : PubMed/NCBI
7	Gauthaman K and Ganesan AP: The hormonal effects of Tribulus terrestris and its role in the management of male erectile dysfunction-anevaluation using primates, rabbit and rat. Phytomedicine. 15:44–54. 2008. View Article : Google Scholar : PubMed/NCBI
8	Qureshi A, Naughton DP and Petroczi A: A systematic review on the herbal extract Tribulus terrestris and the roots of its putative aphrodisiac and performance enhancing effect. J Diet Suppl. 11:64–79. 2014. View Article : Google Scholar : PubMed/NCBI
9	Singh S, Nair V and Gupta YK: Evaluation of the aphrodisiac activity of Tribulus terrestris Linn. In sexually sluggish male albino rats. J Pharmacol Pharmacother. 3:43–47. 2012. View Article : Google Scholar : PubMed/NCBI
10	Chhatre S, Nesari T, Somani G, Kanchan D and Sathaye S: Phytopharmacological overview of Tribulus terrestris. Pharmacogn Rev. 8:45–51. 2014. View Article : Google Scholar : PubMed/NCBI
11	Brown GA, Vukovich MD, Martini ER, Kohut ML, Franke WD, Jackson DA and King DS: Effects of androstenedione-herbal supplementation on serum sex hormone concentrations in 30- to 59-year-old men. Int J Vitam Nutr Res. 71:293–301. 2001. View Article : Google Scholar : PubMed/NCBI
12	Gauthaman K, Adaikan PG and Prasad RN: Aphrodisiac properties of Tribulus Terrestris extract (Protodioscin) in normal and castrated rats. Life Sci. 71:1385–1396. 2002. View Article : Google Scholar : PubMed/NCBI
13	Martino-Andrade AJ, Morais RN, Spercoski KM, Rossi SC, Vechi MF, Golin M, Lombardi NF, Greca CS and Dalsenter PR: Effects of Tribulus terrestris on endocrine sensitive organs in male and female Wistar rats. J Ethnopharmacol. 127:165–170. 2010. View Article : Google Scholar : PubMed/NCBI
14	Rogerson S, Riches CJ, Jennings C, Weatherby RP, Meir RA and Marshall-Gradisnik SM: The effect of five weeks of Tribulus terrestris supplementation on muscle strength and body composition during preseason training in elite rugby league players. J Strength Cond Res. 21:348–353. 2007. View Article : Google Scholar : PubMed/NCBI
15	Antonio J, Uelmen J, Rodriguez R and Earnest C: The effects of Tribulus terrestris on body composition and exercise performance in resistance-trained males. Int J Sport Nutr Exerc Metab. 10:208–215. 2000. View Article : Google Scholar : PubMed/NCBI
16	Brown GA, Vukovich MD, Reifenrath TA, Uhl NL, Parsons KA, Sharp RL and King DS: Effects of anabolic precursors on serum testosterone concentrations and adaptations to resistance training in young men. Int J Sport Nutr Exerc Metab. 10:340–359. 2000. View Article : Google Scholar : PubMed/NCBI
17	Saudan C, Baume N, Emery C, Strahm E and Saugy M: Short term impact of Tribulus terrestris intake on doping control analysis of endogenous steroids. Forensic Sci Int. 178:e7–e10. 2008. View Article : Google Scholar : PubMed/NCBI
18	Yin L and Wang X, Cao X and Wang X: The effects of tribulus terrestris on the time of exhaustion in rats with high intensity training and its mechanism. J Shanghai University Sport. 37:73–77. 2013.
19	Matsumoto T, Sakari M, Okada M, Yokoyama A, Takahashi S, Kouzmenko A and Kato S: The androgen receptor in health and disease. Annu Rev Physiol. 75:201–224. 2013. View Article : Google Scholar : PubMed/NCBI
20	Vingren JL, Kraemer WJ, Hatfield DL, Volek JS, Ratamess NA, Anderson JM, Häkkinen K, Ahtiainen J, Fragala MS, Thomas GA, et al: Effect of resistance exercise on muscle steroid receptor protein content in strength-trained men and women. Steroids. 74:1033–1039. 2009. View Article : Google Scholar : PubMed/NCBI
21	Safarinejad MR, Azma K and Kolahi AA: The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus-pituitary-testis axis, and semen quality: A randomized controlled study. J Endocrinol. 200:259–271. 2009. View Article : Google Scholar : PubMed/NCBI
22	Lee WJ, Thompson RW, McClung JM and Carson JA: Regulation of androgen receptor expression at the onset of functional overload in rat plantaris muscle. Am J Physiol Regul Integr Comp Physiol. 285:R1076–R1085. 2003. View Article : Google Scholar : PubMed/NCBI
23	Aizawa K, Iemitsu M, Maeda S, Otsuki T, Sato K, Ushida T, Mesaki N and Akimoto T: Acute exercise activates local bioactive androgen metabolism in skeletal muscle. Steroids. 75:219–223. 2010. View Article : Google Scholar : PubMed/NCBI
24	Hulmi JJ, Ahtiainen JP, Selänne H, Volek JS, Häkkinen K, Kovanen V and Mero AA: Androgen receptors and testosterone in men-effects of protein ingestion, resistance exercise and fiber type. J Steroid Biochem Mol Biol. 110:130–137. 2008. View Article : Google Scholar : PubMed/NCBI
25	Ratamess NA, Kraemer WJ, Volek JS, Maresh CM, Vanheest JL, Sharman MJ, Rubin MR, French DN, Vescovi JD, Silvestre R, et al: Androgen receptor content following heavy resistance exercise in men. J Steroid Biochem Mol Biol. 93:35–42. 2005. View Article : Google Scholar : PubMed/NCBI
26	Ahtiainen JP, Hulmi JJ, Kraemer WJ, Lehti M, Nyman K, Selänne H, Alen M, Pakarinen A, Komulainen J, Kovanen V, et al: Heavy resistance exercise training and skeletal muscle androgen receptor expression in younger and older men. Steroids. 76:183–192. 2011. View Article : Google Scholar : PubMed/NCBI
27	McMahon CD, Chai R, Radley-Crabb HG, Watson T, Matthews KG, Sheard PW, Soffe Z, Grounds MD and Shavlakadze T: Lifelong exercise and locally produced insulin-like growth factor-1 (IGF-1) have a modest influence on reducing age-related muscle wasting in mice. Scand J Med Sci Sports. 24:e423–e435. 2014. View Article : Google Scholar : PubMed/NCBI
28	Luo L, Lu AM, Wang Y, Hong A, Chen Y, Hu J, Li X and Qin ZH: Chronic resistance training activates autophagy and reduces apoptosis of muscle cells by modulating IGF-1 and its receptors, Akt/mTOR and Akt/FOXO3a signaling in aged rats. Exp Gerontol. 48:427–436. 2013. View Article : Google Scholar : PubMed/NCBI
29	Kim J, Wende AR, Sena S, Theobald HA, Soto J, Sloan C, Wayment BE, Litwin SE, Holzenberger M, LeRoith D and Abel ED: Insulin-like growth factor I receptor signaling is required for exercise-induced cardiac hypertrophy. Mol Endocrinol. 22:2531–2543. 2008. View Article : Google Scholar : PubMed/NCBI
30	Serra C, Bhasin S, Tangherlini F, Barton ER, Ganno M, Zhang A, Shansky J, Vandenburgh HH, Travison TG, Jasuja R and Morris C: The role of GH and IGF-I in mediating anabolic effects of testosterone on androgen-responsive muscle. Endocrinology. 152:193–206. 2011. View Article : Google Scholar : PubMed/NCBI
31	Knapczyk-Stwora K, Grzesiak M, Duda M, Koziorowski M and Slomczynska M: Effect of flutamide on folliculogenesis in the fetal porcine ovary-regulation by Kit ligand/c-Kit and IGF1/IGF1R systems. Anim Reprod Sci. 142:160–167. 2013. View Article : Google Scholar : PubMed/NCBI
32	Lee SH, Johnson D, Luong R and Sun Z: Crosstalking between androgen and PI3K/AKT signaling pathways in prostate cancer cells. J Biol Chem. 290:2759–2768. 2015. View Article : Google Scholar : PubMed/NCBI
33	Kretzschmar K, Cottle DL, Schweiger PJ and Watt FM: The androgen receptor antagonizes Wnt/β-Catenin signaling in epidermal stem cells. J Invest Dermatol. 135:2753–2763. 2015. View Article : Google Scholar : PubMed/NCBI
34	Tarulli GA, Butler LM, Tilley WD and Hickey TE: Bringing androgens up a NOTCH in breast cancer. Endocr Relat Cancer. 21:T183–T202. 2014. View Article : Google Scholar : PubMed/NCBI
35	Wu JL, Leung EL, Zhou H, Liu L and Li N: Metabolite analysis of toosendanin by an ultra-high performance liquid chromatography-quadrupole-time of flight mass spectrometry technique. Molecules. 18:12144–12153. 2013. View Article : Google Scholar : PubMed/NCBI
36	Cavalcanti Gde A, Leal FD, Garrido BC, Padilha MC and de Aquino Neto FR: Detection of designer steroid methylstenbolone in ‘nutritional supplement’ using gas chromatography and tandem mass spectrometry: Elucidation of its urinary metabolites. Steroids. 78:228–233. 2013. View Article : Google Scholar : PubMed/NCBI
37	Kim JH and Thompson LV: Non-weight bearing-induced muscle weakness: The role of myosin quantity and quality in MHC type II fibers. Am J Physiol Cell Physiol. 307:C190–C194. 2014. View Article : Google Scholar : PubMed/NCBI
38	Schilling BK, Fry AC, Chiu LZ and Weiss LW: Myosin heavy chain isoform expression and in vivo isometric performance: A regression model. J Strength Cond Res. 19:270–275. 2005. View Article : Google Scholar : PubMed/NCBI
39	Mitchell CJ, Churchward-Venne TA, Bellamy L, Parise G, Baker SK and Phillips SM: Muscular and systemic correlates of resistance training-induced muscle hypertrophy. PLoS One. 8:e786362013. View Article : Google Scholar : PubMed/NCBI
40	Deschenes MR, Maresh CM, Armstrong LE, Covault J, Kraemer WJ and Crivello JF: Endurance and resistance exercise induce muscle fiber type specific responses in androgen binding capacity. J Steroid Biochem Mol Biol. 50:175–179. 1994. View Article : Google Scholar : PubMed/NCBI
41	Frystyk J: Exercise and the growth hormone-insulin-like growth factor axis. Med Sci Sports Exerc. 42:58–66. 2010. View Article : Google Scholar : PubMed/NCBI
42	Gibney J, Healy ML and Sönksen PH: The growth hormone/insulin-like growth factor-I axis in exercise and sport. Endocr Rev. 28:603–624. 2007. View Article : Google Scholar : PubMed/NCBI
43	Philippou A, Halapas A, Maridaki M and Koutsilieris M: Type I insulin-like growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. J Musculoskelet Neuronal Interact. 7:208–218. 2007.PubMed/NCBI